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439
Korean J. Food Sci. An.
Vol. 33, No. 4, pp. 439~447(2013)
DOI http://dx.do.org/10.5851/kosfa.2013.33.4.439
Applications of Time-Temperature Integrator (TTI)
as a Quality Indicator of Grounded Pork Patty
Ji-Yeon Chun1, Mi-Jung Choi2, Seung Ju Lee3, and Geun-Pyo Hong*
Department of Bio-Industrial Technologies, Konkuk University, Seoul 143-701, Korea1Department of Food Science and Biotechnology of Animal Resources, Konkuk University, Seoul 143-701, Korea
2Department of Bioresources and Food Science, Konkuk University, Seoul 143-701, Korea3Department of Food Science and Technology, Dongguk University-Seoul, Seoul 100-715, Korea
Abstract
Time-temperature integrators (TTIs) are simple and cost-efficient tools which may be used to predict food quality. Enzy-matic TTIs are devised to indicate food quality in the form of color alterations from green to red, based on the cumulativeimpacts of temperature and time period on the enzymatic reactions. In this study, the quality of ground beef patties wasinvestigated for the parameters of pH levels, color, VBN, water holding capacity, and total microbial counts, depending onvarious storage temperatures (5, 15, and 25oC). TTIs were attached to the surface of the ground beef patties in order to eval-uate the degree of correlating colorimetric changes with the determined quality parameters. Through the Arrhenius equa-tion, activation energy and constant reaction rates of TTI, VBN, and total microbial counts were calculated as to observe therelationship between enzymatic reactions of the TTI and food spoilage reactions of the ground beef patties. VBN and totalmicrobial counts were already increased to reach decomposition index (VBN: 20, total microbial count: 7-8 Log CFU/g) ofmeat at middle stage of storage period for each storage temperature. Although activation energy of TTI enzymatic reactionsand food spoilage reactions of the ground beef patties were similar, the change of TTI color was not a coincidence for foodspoilage at 5oC and 15oC of storage temperature. It was suggested that TTI should be designed individually for storage tem-perature, time, type of meat, or decomposition index of meat.
Key words: time-temperature integrator, beef patty, storage, quality indicator
Introduction
Throughout history, food products and services that pro-
mote personal well-being have been sought. Consumers
have demanded quality factors of food especially in the
meat product industry as consumption of meat is gradu-
ally increased. Hence, it is sought to control the quality of
meat at every stage of production, such as the rearing of
the animals, slaughter, distribution and storage. Quality
control is helpful both to the consumer and to the manu-
facturer, because consumer is assured a high quality meat
product and the manufacturer can reduce economic loss
by decreasing unexpected spoilage of meat products
(Bruckner et al., 2013; Taoukis et al., 1999; Vaikousi et
al., 2009).
Temperature-sensitive products are carried through the
cold-chain and are used to check the history of storage
and delivery conditions until the point of consumption.
Many food processing enterprises have applied Hazard
Analysis Critical Control Point system (HACCP) process
to keep up with customer needs. However, it is impracti-
cal to test product qualities such as chemical, physical, or
microbial properties before purchasing in the market.
Consumers can merely confirm that the designated expiry
date is appropriate and personally observe for color, ion
sealed packages, and malodour, when available. (Byeon
et al., 2009; Shin et al., 2006). Moreover, thermal pro-
cessing has been well-known as an effective way of pre-
venting or eliminating photogenic bacteria or viruses
from food products such as meat, fish, and poultry prod-
ucts, but this type of processing is one of the last control
points in HACCP (Orta-Ramirez and Smith 2002; Van
Loey et al., 1996). Obviously, uncooked meat products are
*Corresponding author: Geun-Pyo Hong, Department of Bio-Industrial Technologies, Konkuk University, Seoul 143-701,Korea. Tel: 82-2-450-3674, Fax: 82-2-455-1044, E-mail: [email protected]
ARTICLE
440 Korean J. Food Sci. An., Vol. 33, No. 4 (2013)
exposed to various environmental stresses such as tem-
perature, oxygen, light, and so on, before cooking.
Forecasting systems for food quality have been devel-
oped over past decades. Time-temperature integrators
(TTIs) are used to predict food quality and it has been
considered that it is essential tool in food groups. TTIs are
devised to show food quality as a color alteration which
occurs at varying rates due to exposure to varying temper-
ature. Moreover, TTIs have low-cost and high-efficiency.
(Ellouze et al., 2011; Kim et al., 2012b). Three types of TTI
have been developed, which are based on diffusion, en-
zyme, and polymer sensors, which are classified by reac-
tion material or method. The reaction can be a physical,
chemical or enzymatic irreversible change (Park et al.,
2009; Vaikousi et al., 2009). Vitsab® Smart Labels TTIs,
which are highly efficient and simple, were used in this
study. This TTI is based on enzymatic reaction and uses
lipase. The enzyme induces lipolysis which affects a dec-
rease of pH that causes a color-change of the indicator from
green to red (Kim et al., 2012a; Smolander et al., 2004).
Finally we aim to recognize the state of product quality
through the color of the TTI. There are many instances of
applications of TTI within the food industry (Bobelyn et
al., 2006; Claeys et al., 2002; Giannakourou and Taoukis
2002; Shin et al., 2006; Taoukis et al., 1999; Vaikousi et
al., 2009).
Even if the application of TTIs on food products has
increased because of their cost-effectiveness, simplicity,
and ease-of-use, they still must be calibrated to the chem-
ical, physical, microbial or sensory properties of the prod-
ucts to which they are applied (pH, color, VBN, TBA,
water holding capacity, total microbial count, sensory
evaluation etc.) depending on the storage period and pro-
cessing method (Jeong et al., 2006; Jin et al., 2002; Kim
et al., 2012b; Shin et al., 2006). These methods of determi-
nation take time, cost and skilled technicians to observe
the freshness of meat products, and therefore, it is of great
advantage to carry out a detailed investigation of the rela-
tionship between TTI and quality of meat products, using
the TTI thereafter. In this study, the objective was to inve-
stigate correlation between TTI and ground beef patty
quality. Therefore, we observed changes of TTI’s color
and meat quality such as meat color, pH, VBN, water-
holding capacity, and total microbial count, as measured
during storage under variable temperature conditions.
Arrhenius activation energy was calculated to represent
the correlation between TTI and GBP quality at the same
temperature and period.
Materials and Methods
Materials
Time-temperature integrators (TTI, Vitsab® Smart La-
bels, Sweden) which are an enzymatic reaction type TTI
were donated by Vitsab International. Ground Beef was
obtained from a meat grocery in the Hwayang Market.
Potassium carbonate and Brunswick solution was pur-
chased from SAMCHUN Chemical Co. (Korea). Sulfuric
acid was provided by PFP (PFP Matunoen chemicals Ltd,
Japan) and sodium hydroxide was bought from SHOWA
(SHOWA, Japan). For the microbial test, plate count agar
(PCA) was obtained from Difco (Becton Dickinson and
Company, USA).
Sample preparation
Seventy grams of ground beef was formed using a petri
dish (Internal dimension: 85.6 mm × 12.6 mm, SPL, Korea)
to result in a uniform and reproducible sample shape and
volume. TTIs were attached to the middle of the surface
of the ground beef patties (GBPs). GBPs with attached
TTI were then stored at 5oC, 15oC, or 25oC for predeter-
mined storage periods. Change in GBPs quality and TTI
was observed at certain periods in triplicate. Observations
of GBPs quality ceased when the a*-value of TTIs (1st
condition) was over 20-25, or when VBN (2nd condition)
was greater than 20, which was based on the findings of
a previous research (Chun et al., 2009).
Color
CIE Lab color values were measured from the surface of
GBPs with a color reader (CR-10, Konica Minolta Sens-
ing Inc., Japan) which was calibrated using a standard
white plate. The CIE L*, a*, and b* values were designa-
ted as indicators of lightness, redness, and yellowness, res-
pectively. The samples were determined and three meas-
urements were taken from the surface of each sample. a*-
values were then considered as quality attribute depend-
ing on storage temperature. The change of a*-value was
calculated over time to evaluate the constant reaction rate
and activation energy, using the Arrhenius equation.
Volatile basic nitrogen (VBN)
VBN of samples was measured by Conway’s Micro dif-
fusion method of Korean Food Standards Codex (KFDA,
2012). Three Conway’s tools were cleaned with a neutral
detergent to remove any containment. To the edge of the
outer ring of each unit was applied sealing agent. Five
Applications of TTI as Meat Quality Indicator 441
grams of GBP from a homogenate was mixed with 25 mL
distilled water and was then filtered. The 1 mL of filtrate
was put into the lower part of outer ring and 1 mL of sat-
urated K2CO
3 solution was carefully pipetted into the upper
part of outer ring. One mL of 0.01 N H2SO
4 was added to
the inner ring of the unit and immediately the units were
covered and closed with clip. Solution of outer ring was
mixed carefully to prevent any entering the inner ring.
The Conway diffusion cell was filled with the filtrate of
GBPs and was kept at 25oC for 1 h. One drop of Brun-
swick solution was added to the inner ring of the unit and
the filtrate of GBPs was then titrated with 0.01 N NaOH
solution. The VBN value was calculated as
where a was amount (mL) of 0.01 N NaOH solution for
filtrate of GBPs, b was amount (mL) of 0.01 N NaOH
solution for control, d was dilution factor, W was GBPs
amount (mg) and f was titer of 0.01 N NaOH solution.
pH
Five grams of GBP was mixed with 20 mL of water and
was homogenized at 10,000 rpm for 3 min using SMT pro-
cess homogenizer (SMT Co. Ltd., Japan). The pH of GBPs
was measured in triplicate using a pH meter (pH 900,
Precisa Co., Swiss).
Water holding capacity
Water holding capacity (WHC) of GBPs was determined
(Hong et al., 2008). One gram of GBP was weighed and
placed in a centrifuge tube along with gauze as an absor-
bent. The samples were centrifuged for 10 min at 3,000
rpm and 4oC in a refrigerated centrifuge (RC-3, SORVALL
Co., USA). After centrifuging, the meat was removed from
the tube and the weights of the centrifuge tubes before and
after drying were determined. WHC was expressed as the
percentage of moisture remaining in GBP samples. All
measurements were carried out in triplicate.
Total microbial count
The total microbial count of GBPs stored at 5oC, 15oC,
and 25oC was determined at certain periods. One gram of
sample was diluted in 9 mL pre-sterilized 0.85% NaCl solu-
tion. One milliliter of bacteria solution was inoculated on
the surface of a PCA plate. The plates were incubated at
37oC in incubator for 24-48 h. Determination of CFU/g
was then carried out.
Correlation of TTI, VBN, or total microbial count
by Arrhenius equation
Specially, the a*-value of TTI, VBN and total micro-
bial count of GBPs kept at various storage temperatures
was calculated by Arrhenius equation. The Arrhenius equa-
tion defines the quantitative basis of the relationship bet-
ween the activation energy (Ea) and constant reaction rate
(k) as
where R is the universal gas constant (8.314 J/mol·K) and
T is absolute temperature (K).
The Ea of TTI, VBN, or total microbial count depending
on various storage temperatures was calculated and plot-
ted against the reciprocal of absolute temperature accord-
ing to Eq. 1. The activation energy was then calculated
from the logarithmic form of the Arrhenius equation. The
parameter Ea was calculated as a slope by plotting lnk as
a function of 1/T according to the following equation.
Statistical analysis
The data were analyzed by using one-way analysis of
variance with storage periods. An analysis of variance was
performed on all the variables using the General Linear
Model (GLM) procedure (SAS 9.3, SAS Institute, USA).
Differences among the means were compared using Tukey's
Studentized Range (HSD) Test (p<0.05).
Results and Discussion
Color
As described at sample preparation, the a*-value of the
TTI or VBN were investigated as representative factors to
indicate food spoilage in previous study. Through the pre-
vious study, all observation of GBPs’ characteristics such
as color, VBN, pH, water holding capacity, and microbial
test was finished when the a*-value of TTI was 20-25.
Fig. 1 shows that changes in the a*-value of both TTI and
GBPs occurred during storage periods. TTI was kept at
25oC, 15oC, or 5oC and color observation were finished
after 24 h, 196 h and 288 h respectively according to the
a*-value (20-25). The total storage period was also sub-
divided into initial stage, middle stage, and final stage,
because each sample temperature had different a storage
VBN mg%( ) 0.14b a–( ) f×
W---------------------× 100× d×=
k AEa
RT-------–⎝ ⎠
⎛ ⎞exp=
kln AlnEa
R-----
1
T---–=
442 Korean J. Food Sci. An., Vol. 33, No. 4 (2013)
period (Table 1). The a*-value of TTI only was signifi-
cantly increased by raising the storage temperature at 25oC
and 15oC (p<0.05), however, it was no difference among
samples at 5oC storage temperature until VBN was over
20. There was no remarkable change in the a*-value of
GBPs kept at 15oC or 5oC. The b*-value of TTIs (Fig. 2)
fluctuated during the storage period and the b*-value of
GBPs was quite stable at around 10 to 14 (p>0.05). The
L*-value was not changed during storage periods (results
not shown). Fig. 3 shows the real color of TTI and GBPs.
TTI was changed green-yellow-red and GBPs were chan-
ged form blood red-light brown-deep blood red, in order
of storage period, except for 5oC storage temperature. The
a*-value was the most changeable factor to indicate and
predict the state of food quality, and moreover, consumers
may easily recognize this TTI color change (Byeon et al.,
2009; Chun et al., 2009; Kim et al., 2012a).
Volatile basic nitrogen (VBN)
The VBN value of GBPs depended on storage temper-
ature (5oC, 15oC, and 25oC). VBN value was increased with
storage period. It was quickly and steadily increased up to
22 mg% at 21 h with 25oC of storage temperature (Fig.
4A). Interestingly, VBN was dramatically increased at 75 h
at 15oC and 5oC of storage temperature (Fig. 4B). The a*-
value was very low at the same time for both storage tem-
peratures but the VBN of GBPs was already over 20 mg%
at the 15oC storage temperature. A VBN value of 20 mg%
is the prescribed point of spoilage according to the Korean
Food Standards Codex. (Korea Food & Drug Administra-
tion, 2012). Likewise 5oC storage temperature did not
much affect the decomposition of GBPs, but VBN was
increased up to 19.3 mg% during the storage period (Fig.
Fig. 1. a*-value of TTI or meat as storage temperature (A: 25oC, B: 15oC, C: 5oC). Vertical bars indicate standard deviations (n=3).
Table 1. Storage period of TTI and ground beef patty depend
on storage temperature
Storage
temperature (oC)
Storage time (h)
Initial stage Middle stage Final stage
25 0 12 24
15 0 96 192
5 0 144 288
Applications of TTI as Meat Quality Indicator 443
4C). In this study, storage temperature was determined to
be a more influential factor in increasing VBN than stor-
age time.
Fig. 2. b*-value of TTI or meat as storage temperature (A: 25oC, B: 15oC, C: 5oC). Vertical bars indicate standard deviations (n=3).
Fig. 3. Change in color of TTI and ground beef patty during storage periods.
444 Korean J. Food Sci. An., Vol. 33, No. 4 (2013)
pH
In this study, the pH of GBPs stored at 25oC ranged bet-
ween 5 and 5.4 during storage periods and there was no
big difference, but there was significant difference during
storage period (p<0.05)(Fig. 5). At 15oC storage tempera-
ture, initially the pH of GBPs was decreased and then in-
creased up to 6.9 from middle stage to final stage. How-
ever, the pH of GBPs was not changed at 5oC during stor-
age periods (p>0.05). And the pH of GBPs stored at 15oC
storage temperature as storage periods up to 6.77. Fresh
meat is generally regarded as having a pH of 5.5-5.8 dur-
ing storage. When pH of meat reaches pH 8, meat is re-
garded as being fully decomposed (Shin et al., 2006). GBPs
kept at 15oC were almost spoiled at final stage of storage
period based on their pH. The GBPs kept at 5oC were not
decomposed because of the low storage temperature. GBPs
kept at 25oC were also not changed significantly because
the storage periods was too short for sufficient chemical
reaction of free amino acids and proteolysis by microor-
ganism to take place, although the temperature was high
enough to affect other quality parameters of GBPs (Kim
and Lee, 2011). Low storage temperature (< 5oC) did not
greatly affect pH as previously decomposed in several
Fig. 4. VBN value of GBPs as storage temperature (A: 25oC, B: 15oC, C: 5oC). Vertical bars indicate standard deviations (n=3).
Fig. 5. pH of GBPs kept at various temperatures during stor-
age periods. Vertical bars indicate standard deviations
(n=3). Means with different letters are significantly dif-
ferent (p<0.05).
Applications of TTI as Meat Quality Indicator 445
studies (Jeong et al., 2006; Jeremiah and Gibson 2001).
Holley et al. (1994) also observed that the pH of fresh
meat increased with the storage period. Storage time is
more influential in increasing the pH of food compared to
storage temperature.
In the study of Shin et al. (2006), the pH of beef loin or
pork belly kept 2oC was coincide with the freshness indi-
cator which was pH sensitive. Likewise, the a*-value of
TTI kept at 15oC was associated with pH in this study.
However, other TTI treatments at 25oC and 5oC were not
mat- ched with pH of GBPs. The a*-value of TTIs kept
25oC rose quickly up to 26 with a red color, which indi-
cated the spoilage stage, but the pH remained within the
stable region, under 5.5. In the case of the 5oC TTI treat-
ment, there was no change in either the a*-value (Green
TTI color) or the pH until the final stage, the point at
which the VBN of GBPs was determined to be 20 mg%.
Water holding capacity
Water holding capacity ranged from 65% to 75% (Fig.
6). Even if there was no significant difference among sam-
ples or storage periods (p>0.05), samples stored at higher
temperature had relatively higher water holding capacity
during storage periods. Generally, water holding capacity
is affected by storage temperature, rigor development, pH
decline rate, ionic strength, and oxidation. In other words,
isoelectric point (pI), low pH, or high storage temperature
induce a reduction in water holding capacity (Huff-Lon-
ergan and Lonergan, 2005). In this study, although the pH
of GBPs was maintained at 25oC was in pI zone, water
holding capacity of GBPs was not changed significantly
at all storage temperature furthermore it was even higher
than others during storage periods (p>0.05). At the final
storage period, although the pH of GBPs was stable dur-
ing storage period at 25oC, water holding capacity was
decreased to 66%, which was one of the lowest value.
The reason was that the storage period (24 h) at 25oC was
likely too short to affect the pH of the GBPs properties.
Microbial observation
Total microbial count of GBPs was counted during sto-
rage periods at 5oC, 15oC, and 25oC (Fig. 7). Initial spoil-
age is important when we observe the behavior of micro-
organism. Although initial total microbial count was quite
high to do microbial test in all GBPs, the difference was
a clearly observed among GBPs in this study. As depicted
in Fig. 7, microorganisms significantly and gradually inc-
reased at 15oC and 25oC storage temperature during stor-
age periods (p<0.05). Whereas the population of the 5oC
treatment was relatively well controlled until 96 h storage
however, it was dramatically increased after reaching 7
Fig. 6. Water-holding capacity GBPs kept at storage tempera-
tures during storage periods. Vertical bars indicate stan-
dard deviations (n=3). Means with different letters are
significantly different (p<0.05).
Fig. 7. Total microbial counts of GBPs during storage periods.
Vertical bars indicate standard deviations (n=3). Means
with different letters are significantly different (p<0.05).
446 Korean J. Food Sci. An., Vol. 33, No. 4 (2013)
Log CFU/g (p<0.05). In the study of Jeong et al. (2006)
two grades of beef were stored at 1oC. Total bacterial
count reached 8 Log CFU/g at 28 d of storage. In the
study of Shin et al. (2006), beef loin and pork belly were
kept at 2oC for 10 d. Total aerobic bacteria of beef loin
was 8 Log CFU/g at 10 d. Jeong et al. (2006) and Shin et
al. (2006) supposed that the increase of microorganisms
was temperature dependant.
However, each GBP sample was determined as 7 to 8
Log CFU/g at the middle stage of VBN development.
Generally, over 8 Log CFU/g of microorganism make
food to be decomposed and cause putrefied flavor which
is unfavorable (KFDA, 2012). Therefore, the total micro-
bial count cannot be observed through the basic senses
until the meat is in the final stages of spoilage.
TTI color, VBN or Total microbial count of meat, as
described by Arrhenius equation
Constant reaction rate (k) and activation energy (Ea) of
TTI (color, a*-value), quality of GBPs (VBN) or micro-
bial growth (total microbial count) depend on storage tem-
perature, and this was calculated through the Arrhenius
equation (Fig. 8 and Table 2). The k of TTI color, VBN,
and total microbial count each developed at increasing
rates with increasing storage temperature. The k of VBN
was highest at every storage temperature. As a result of
VBN determinations, every GBPs started to be spoiled at
near middle stage of each samples in this study. The Ea of
TTI, VBN, and total microbial count were similar as 95.12,
92.60 or 93.90 kJ/mol, respectively. The Ea of VBN and
microbial growth were in the range of typical Ea values for
food quality losses (Labuza, 1982). If there is more than
±25 kJ/mol of Ea differences between food and TTI, the
accuracy of indicator is regarded as poor (Park et al., 2013;
Taoukis, 2001; Wanihsuksombat et al., 2010). Moreover,
the Ea of food is changed depending on the temperature
interval (Wanihsuksombat et al., 2010). In this study, even
though Ea
was similar between the TTI and the deter-
mined quality parameters of GBPs, it did not coincide with
the decomposition or spoilage of GBPs. This problem has
been a major disadvantage of enzymatic TTIs for food
shelf life in the past, but such systems may best fitted to
their optimum foods as well as reverse engineered to some
degree. (Byeon et al., 2009; Kim et al., 2012a; Kim et al.,
2012b; Park et al., 2013; Taoukis et al., 1999).
Conclusions
It was investigated whether a TTI was appropriate for
the prediction of quality of GBPs, such as VBN or total
microbial count at 25oC. However, there was insufficient
correlation with the color change of the TTI at 5oC and at
15oC, although the interrelation between the TTI and the
index of GBPs quality such as pH, VBN, and total micro-
bial count was slightly observed. In other words, one type
of TTI could not indicate quality of GBPs kept in various
storage conditions. It has been suggested that TTIs should
be designed individually depending on storage tempera-
ture, time, and the type of meat. Moreover, meat quality
must be investigated because it may not be possible to
simultaneously match various attributes of meat quality
with the reaction of a single TTI.
Acknowledgements
This work was performed as a research project of the
iPET (Korea Institute of Planning and Evaluation for Te-
chnology of Food, Agriculture, Forestry and Fisheries) sup-
ported by Ministry for Food, Agriculture, Forestry and Fi-
sheries of Korea. This study was also partially supported
by the SMART Research Professor Program of Konkuk
University, Seoul, Korea.
Table 2. Arrhenius parameters, activation energy (Ea) and
Constant reaction rate (k) of TTI, VBN or total
microbial count with different storage temperature
T (oC) k Ea (kJ/mol) R2
TTI
25 0.099
95.1 0.81915 0.008
5 0.006
VBN
25 0.685
92.6 0.91015 0.396
5 0.048
Total
microbial
count
25 0.090
93.9 0.90915 0.011
5 0.006
Fig. 8. Arrhenius plot of the constant reaction rate (k) of TTIs
with various storage temperatures.
Applications of TTI as Meat Quality Indicator 447
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(Redeived 2013.4.17/Revised 2013.6.21/Accepted 2013.7.5)